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Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. MATERIALS and METHODS
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Using three sampler devices (SAS, Andersen Six-Stages and All Glass Impinger), the environmental impact of bacterial and fungal aerosols generated by municipal wastewater treatment plants operating with different methods of sludge oxygenation were evaluated. The highest microbial concentrations were recovered above the tanks (2247 cfu m−3) and in downwind positions (1425 cfu m−3), where a linear correlation (P < 0·05) was found between the quantity of sewage treated and the entities of microbial aerosol dispersion. Moreover, an exponential increase (P < 0·05) in the bacteria recovered from the air occurred at increasing times of treatment. However, after long-term plant operation, high bacterial and fungal concentrations were found in almost all of the sites around the plant. Coliforms, enterococci, Escherichia coli and staphylococci were almost always recovered in downwind positions. Considerable fractions (20–40%) of sampled bacteria were able to penetrate the final stages of the Andersen apparatus and thus, are likely to be able to penetrate the lungs. The plant operating with a fine bubble diffused air system instead was found to generate rather low concentrations of bacteria and fungi; moreover, staphylococci and indicator micro-organisms were almost absent. Finally, salmonellae, Shigella, Pseudomonas aeruginosa and Aeromonas spp. were not detected in either of the plants. The results indicate a remarkable dispersion of airborne bacteria and fungi from tanks in which oxygen is supplied via a mechanical agitation of sludge, and suggest the need to convert them to diffused aeration systems which pose a lesser hazard for human health.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. MATERIALS and METHODS
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Aerosols containing micro-organisms may be generated through natural processes and by human activity. It has been reported that aerosols are capable of transporting micro-organisms over long distances ( Bovallius et al. 1978 ) and, depending on the source, that they may be able to produce infections ( Fraser 1980; Sattar and Ijaz 1987), asthmatic problems ( Gravesen 1979) and other health effects ( Jacobs 1989; Burrel 1990) in susceptible subjects. The aeration tanks of wastewater treatment plants are recognized as important sources of microbial aerosols ( Napolitano and Rowe 1966; Kenline and Scarpino 1972; Cannon 1983; Fannin et al. 1985 ) and therefore might be hazardous for exposed subjects, firstly for plant workers as a consequence of direct contact with the contaminated materials/substrates or by inhalation of aerosolized micro-organisms. Moreover, a potential risk for visitors to the plants and for the surrounding population cannot be excluded. Various potentially infectious agents have frequently been recovered from the air around wastewater plants ( Hickey and Parker 1975; Millner et al. 1980 ; Fannin et al. 1985 ) and a high prevalence of antibodies against several enteric viruses has been found in exposed subjects ( Clark 1981a; Heng et al. 1994 ), although this is not necessarily related to aerosols. Clear evidence of the adverse health effects caused by exposure to micro-organism-containing aerosols, however, has not yet been presented in a satisfactory manner ( Clark et al. 1981b ; Stener 1986; Maguire 1993), and as far as is known, outbreaks due to aerosols generated during the wastewater treatment process have never been reported. Furthermore, the health risks for populations living near wastewater treatment plants remain poorly investigated. The aim of the present study was to obtain more information about the environmental microbial dispersion from wastewater treatment plants by evaluating the densities and types of airborne bacteria and fungi recovered in the vicinity of the aerated tanks. For this purpose, two different plants were selected. The first is operative only in the summer and uses a mechanical agitation for the aeration of the settled sewage. The other is operative year-round and the oxygen for sewage aeration is supplied via a fine bubble diffused air system.

MATERIALS and METHODS

  1. Top of page
  2. Abstract
  3. Introduction
  4. MATERIALS and METHODS
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Wastewater treatment plants

Two wastewater treatment plants located along the north-west Adriatic coast were studied. The first (hereafter referred to as Plant A) is operative only in the summer and receives 7500 m−3 d−1 of wastewater during its peak of activity, equivalent to about 30 000 inhabitants. This plant uses a mechanical aeration of settled sewage (activated sludge process). The second plant (Plant B) operates continuously throughout the year and treats 15 500 m−3 d−1 of sewage in winter, 16 000 m−3 d−1 in spring and 22 000 m−3 d−1 in summer, corresponding to the equivalent of about 62 000, 64 000 and 88 000 inhabitants served, respectively. The oxygen in the tanks is supplied by a fine bubble diffused air system.

The sampling of aerosols was carried out near the wastewater aeration tanks as follows: in summer at different periods before and after start-up of the process in Plant A; and in winter, spring and summer in Plant B.

Air samplers and micro-organisms assayed

Three different samplers were employed for the detection and enumeration of aerosolized micro-organisms. The SAS (Surface Air System) impactor aspirates air at a fixed speed (180 l min−1) for a variable time onto a 55 mm contact plate filled with appropriate agar medium. All aerosol samples were collected after determination of the wind direction; the sites were at a distance of 2 m upwind, 2, 10 (Plant B) and 20 (Plant A) m downwind, and 2 m laterally, with respect to wind direction. The sampling time used varied from 30 s to 2 min, depending on the supposed microbial concentration in the air. The micro-organisms sampled were total bacteria and fungi, total coliforms, enterococci, Escherichia coli and staphylococci.

The Andersen Six-Stage Viable Particle Sampler (hereafter Andersen) contained six Petri dishes filled with an appropriate agar medium. Each stage has 400 holes with diameters that range from 1·81 mm in the first stage to 0·25 mm in the sixth stage. Aerosol samples were collected 1·5 m above and 2 m downwind of the aeration tanks. The sampling time was 20 min, with a constant sampling flow rate of 28·5 l min−1. The sampler was used to evaluate the total bacterial count.

The All Glass Millipore Impinger (hereafter Impinger) containing appropriate enrichment broth medium was positioned 2 m downwind from the tanks. The sampling time was 30 min with a flow ratio of 12·5 l min−1. This sampler was used to collect salmonellae, Shigella, Aeromonas spp. and Pseudomonas aeruginosa.

All collected samples were transported to the laboratory within 3–4 h of sampling and were incubated at 37 °C for bacterial counts, at 20 °C for fungal counts and at 45 °C for E. coli counts. The results are expressed as the number of colony-forming units per cubic metre (cfu m−3) of air.

At the same time as aerosol sampling, the temperature and relative humidity were monitored, using an aspirated psychrometer, and wind speed, by an anemometer.

Culture media

The solid culture media were tryptic glucose yeast agar (Oxoid) for total bacterial counts, Sabouraud dextrose agar (Oxoid) for total fungal counts, violet red bile lactose agar (Oxoid) for total coliforms and E. coli, Bacto m. enterococcus agar (Difco) for enterococci, mannitol salt agar (Oxoid) for staphylococci (colonies grown in this agar were processed for the coagulase test using the Staphytect plus, Oxoid), SS agar modified (Oxoid) for salmonellae and Shigella, m-Aeromonas selective agar (Biolife) for Aeromonas, and pseudomonas CN medium (Oxoid) for Ps. aeruginosa. The liquid enrichment media used for Impinger were selenite cystine broth (Oxoid) for salmonellae and Shigella, nutrient broth (Oxoid) for Ps. aeruginosa and alkaline peptonate water for Aeromonas.

Statistical analyses

A linear and exponential regression (both evaluated by anova) and a Spearman rank correlation were used.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. MATERIALS and METHODS
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The results on airborne bacteria and fungi recovered from Plant A are shown in Fig. 1. Before the plant was started up (Period A), the concentrations of total bacteria and fungi was found to be very low in all five positions selected. Enterococci were not detected while coliforms and staphylococci were only rarely recovered during sampling. After plant operation commenced (Periods B–E), a progressive increase in the presence of aerosolized micro-organisms was found. The highest concentrations were recovered at the sites 2 m (Position 4) and 20 m (Position 5) downwind. Furthermore, analyses of data obtained in the downwind positions showed a statistically significant correlation (P < 0·05) between the total viable bacterial and fungal counts obtained and the corresponding quantity of sewage being treated ( Fig. 2). From analysis of panels (a) and (b) in Fig. 1, it can be seen that the greatest concentrations of bacteria and fungi were found about 4 weeks after the start of the process (Period E), corresponding to maximum activity of the plant (7500 m−3 d−1 sewage treated). Total bacterial counts ranged from 444 cfu m−3 laterally with respect to the tanks, to 560 cfu m−3 downwind, while fungal concentrations ranged from 660 to 1110 cfu m−3 in the same positions. It is interesting to note that with increasing time from the start-up of activity, microbial aerosol dispersion appeared to become more uniformly distributed around the tanks. Total coliforms and enterococci showed a similar pattern, although to a different degree, of total bacterial and fungi aerodispersion, while E. coli was recovered only in Periods C–E. Staphylococci were constantly recovered at the downwind positions in concentrations that increased, as it did for the other species of bacteria, with the time that the plant had been running; 16–40% of colonies were identified as staphylococci coagulase + and therefore were probably Staph. aureus. Finally, temperature (ranging from 24 to 27 °C), humidity (from 53 to 77%) and wind speed (from 1·5 to 4 m s−1), were shown to be quite similar during the different periods of sampling.

image

Figure 1. Total bacterial and fungal counts, coliforms, enterococci, Escherichia coli and staphylococci recovered from Plant A. All the values represent the mean of three separate air samplings performed with the SAS instrument and are expressed as cfu m−3. Positions: 1 (□) = 2 m upwind, 2 (▨) and 3 (▧) = 2 m, respectively, on the right and on the left with respect to the wind direction, 4 (░) and 5 (▪) = 2 and 20 m downwind, respectively. Periods: before (A) and 1 (B), 3 (C), 12 (D) and 25 (E) days after plant activity was started. (a) Total bacterial count; (b) total fungal count; (c) total coliforms; (d) enterococci; (e) Escherichia coli; (f) staphylococci

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image

Figure 2. Correlation between the concentrations of airborne bacteria [(a) and (b)] and fungi [(c) and (d)] and the amount of sewage treated. Air was sampled with the SAS at 2 m [(a) and (c)] or 20 m downwind [(b) (d)] of Plant A

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A second set of experiments was performed with the Andersen apparatus above the platforms and at 2 m downwind from the tanks of Plant A. As shown in Table 1, the concentration of total bacteria in the aerosols was already high, especially on the platforms, just a few days after the process had started. Using an exponential regression +anova test, it was observed that there was an exponential increase in the cfu m−3 with time, both above the tank (P = 0·019) and 2 m downwind (P = 0·01). When the same test was applied taking into account the quantities of sewage treated rather than time, the results were not significant (P > 0·05). The same result was also obtained with the SAS data (P = 0·009) in the 2 m downwind position. This would suggest the importance of time in determining the microbial aerosol concentration. Comparing the data obtained with SAS ( Fig. 1) with those obtained with the Andersen sampler ( Table 1) at the same time at 2 m downwind, it is of note that the bacterial counts were higher by Andersen sampling, suggesting that this device is more efficient in collecting viable bacteria. As shown in Table 1, the percentage of bacteria able to reach the 5th and 6th stages of the Andersen apparatus ranged from about 20 to 40% of the total bacteria sampled, and these percentages were not correlated (P = 0·39, Spearman rank correlation test) with the amount of total bacteria sampled.

Table 1.  Total bacterial counts obtained sampling with the six-stage Andersen device above and 2 m downwind from Plant A before and after the start-up of plant activity *
Above the tank2 m downwind
Six stages5th + 6th stageSix stages5th + 6th stage
Periodnn%nn%
  1. *Results are expressed as cfu m −3 and represent the mean of three experiments that agreed within 15% of the reported values.

Before913538·4853541·1
After 1 day81717221·037415541·4
After 3 days148949433·165715523·6
After 12 days224763528·2142540528·4
After 25 days162332920·2108137834·9

All the sampling performed with the Impinger device in Plant A gave negative results for isolation of salmonellae, Shigella, Ps. aeruginosa and Aeromonas spp. Sampling (250 l of air each time) was repeated three times for each period at 2 m from the tanks in the downwind position.

In Plant B, which uses a fine bubble diffused air activated sludge process and is continuously operative, the aerosols were sampled with SAS at 2 m upwind, and 2 m and 10 m downwind, in winter, spring and summer. As shown in Table 2, the concentrations of both total bacteria and fungi, and of the various bacterial species studied, were markedly lower or absent compared with those recovered in the same positions at Plant A. As for Plant A, the highest concentrations of bacteria and fungi were collected at the site 2 m downwind from the tanks, i.e., 298 and 222 cfu m−3 bacteria, and 147 and 190 cfu m−3 fungi, in winter and summer, respectively. Escherichia coli, total coliforms and enterococci were not detected, with the exception of coliforms found 10 m downwind in winter, and one occasion when enterococci were found 2 m downwind in spring. Staphylococci were only recovered downwind and in low numbers. The lower airborne bacterial concentrations near Plant B were also confirmed using the Andersen sampler (not shown).

Table 2.  Mean micro-organisms concentrations recovered with the SAS in different seasons and sampling sites in Plant B *
Seasons
Micro-organismsPositionsWinterSpringSummer
  • *Results are expressed as cfu m −3 and represent the mean of three experiments that agreed within 15% of the reported values.

  • Value of a single sampling.

Total bacterial count2 m upwind8·95·566·6
2 m downwind298·811·1222
10 m downwind170·511·1105·4
Total fungal count2 m upwind27·538·892
2 m downwind147·238·8190
10 m downwind62·338·8106
Total coliforms2 m upwindndndnd
2 m downwindndndnd
10 m downwind1·3 ndnd
Enterococci2 m upwindndndnd
2 m downwindnd2·7 nd
10 m downwindndndnd
Escherichia coli2 m upwindndndnd
2 m downwindndndnd
10 m downwindndndnd
Staphylococci2 m upwindndndnd
2 m downwind12·420·824·9
10 m downwind6·98·311·1

As in the case of Plant A, salmonellae, Shigella, Ps. aeruginosa and Aeromonas spp. were not recovered with the Impinger.

Comparing the data obtained in Plant A with those for Plant B, it is clear that higher concentrations of aerosols containing micro-organisms were generated from the tanks of the first plant, probably as a consequence of the mechanical aeration of the sludge. To test this hypothesis, the data obtained for Plant B in this study were compared with those obtained for the same plant in an earlier study ( Brandi et al. 1993 ) when mechanical oxygenation was used for the digestion process. As shown in Table 3, total bacterial and fungal counts, coliforms and staphylococci were recovered to a much greater extent at the same positions and seasons when the sludge was mechanically aerated.

Table 3.  Influence of the sludge oxygenation system on the dispersion of microbial aerosols from Plant B *
Season
SpringSummer
2 m10 m2 m10 m
 Mech Bubbl MechBubblMechBubblMechBubbl
  • *Samplings were performed with SAS at downwind positions and are expressed as cfu m −3. The values referring to Bubbl. were obtained in a previous study ( Brandi et al. 1993 ) and represent the mean of three experiments for each season and sampling site that agreed within 15%.

  • Aeration of the sludge: Mech = mechanical agitation, Bubbl = fine bubble diffused air.

Total bacterial count483·311·1274·911·11816·6222·01383·3105·4
Total fungal count541·638·8816·638·82900·0190·05000·0106·0
Staphylococci25·920·825·08·3100.024·9183·311·1
Total coliforms75·2037·20966·60366·60
Escherichia coli000054·1016·60

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. MATERIALS and METHODS
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Airborne micro-organisms generated from wastewater treatment plants may be a potential source of a wide variety of health hazards ( Hickey and Parker 1975). Therefore, to ensure the health of plant workers and local residents, it is also necessary to evaluate the presence and concentrations of airborne micro-organisms in the proximity of the plants. With this aim, a study was conducted to evaluate the different factors influencing the microbial concentrations of aerosols liberated from the aeration tanks. In order to determine the importance of the oxygenation systems used, one plant was selected that uses mechanical agitation for aeration of the sludge and another in which the oxygen was supplied with a fine bubble diffused air system. Furthermore, as the former plant was operative only in the summer, serving a mainly tourist population, it was possible to distinguish the type and quantity of microbial pollution due to the wastewater treatment from the microbial background of the air in the specific area.

From the data reported in this paper it is clear that the type of aeration used in the activated sludge process markedly influences the microbial content of the air around the plant. Mechanical agitation of the sludge generates aerosols with high concentrations of bacteria and fungi. It is interesting to note that when the plant reached its peak of activity, high concentrations of airborne bacteria and fungi were seen as far as 20 m downwind of the tank and 2 m laterally with respect to the wind direction. This would suggest that when the digestion process is fully operative, a potential risk for human health may exist at almost all the sites around the plant. Consistent with this supposition was the presence of coagulase positive staphylococci and indicator micro-organisms (coliforms, E. coli, enterococci) found above all in the downwind positions.

From a comparison of data obtained with the different samplers, it is evident that the Andersen was more efficient than the SAS in collecting bacteria from the air. This discrepancy was not unexpected as both field and laboratory studies have frequently reported considerable differences among the density of collected micro-organisms measured with different sampling devices ( Jensen et al. 1992 ). Furthermore, several factors can contribute to underestimation of the bacterial concentration in aerosols. First of all, underestimation due to a colony masking effect (colony overlap) should be considered ( Chang et al. 1994 ). Furthermore, during sampling, microbial damage may occur due to the impact of the cells on the agar, affecting the viability and culturability of collected micro-organisms ( Stewart et al. 1995 ). It is reasonable to assume that the degree of microbial injury will increase with airflow speed. This would explain, at least in part, the lower cfu counts obtained here with SAS, which samples airspeeds 6·3-fold higher than with the Andersen.

The aim of using the Andersen sampler, however, was also to obtain information on cell density and particle size ( Andersen 1958). As this sampling device sizes the airborne particles by collecting them in different stages, it is possible to measure the fraction of respirable particles with the potential to reach the alveoli. It was observed that this fraction was already greater than 20% (median 30·7) of the collected bacteria. However, the percentage of bacteria able to penetrate the lungs was not correlated with the degree of aerosol contamination. This would suggest that the risks associated with exposure to aerosols could be closely related not only to the density but also to the type of aerosolized particles.

In view of the problem of bacterial damage due to agar impact and/or cellular dessication on the agar surface as a result of long exposure to airflow, it is thought that neither the Andersen nor the SAS devices can be used efficiently for sampling bacterial species, such as pathogenic bacteria, that may be present in very low concentrations in aerosols. Therefore, to overcome this limitation, a bioaerosol sampler (Impinger) was selected which uses a liquid medium for micro-organism collection, although the device was still unable to recover salmonellae, Shigella, Aeromonas spp. and Ps. Aeruginosa.

An increasing number of reports have recognized the presence of bacteria, including various human enteric pathogens (e.g. Salmonella enteritidis, Shigella, enterotoxic E. coli, Vibrio cholerae) from several substrates in a viable but non-culturable state ( Roszak et al. 1984 ; Islam et al. 1993 ; Cappelier et al. 1999 ). The presence of viable but non-culturable pathogenic bacteria in aerosols should not be excluded.

In conclusion, wastewater treatment plants operating with mechanical aeration have an environmental impact that is clearly unfavourable, due to high dispersion around the tanks of aerosols containing micro-organisms. On the contrary, aerobic digestion with a submerged microbubble system seems to pose little risk from airborne transmission of pathogenic bacteria and fungi to waste-treatment workers and local residents. For this reason, the conversion of mechanical oxygenation systems to submerged oxygenation systems of the sludge should be considered.

Although it is difficult to evaluate the precise contribution of microbial aerosols generated from tanks to human illness, determination of the micro-organism content and presence of pathogenic species in air at the wastewater treatment plant site may provide an insight into their potential adverse health effects.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. MATERIALS and METHODS
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The authors thank M. Rocchi for his support in performing the statistical analyses. This research was supported by Italian Ministry of University and Scientific and Technological Research.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. MATERIALS and METHODS
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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